'Tarwi' (Lupinus Mutabilis Sweet)

Crimson Publishers Review Article Wings to the Research

The Andean Lupine-‘El Chocho’ or ‘Tarwi’ (Lupinus mutabilis Sweet)

Doris Chalampuente-Flores1,2, César Tapia Bastidas2 and Marten Sørensen3*

1 ISSN: 2637-7802 University Santiago de Compostela, Spain 2Technical University of the North, Ecuador, National Institute of Agricultural Research, Ecuador 3Department of Plant & Environmental Sciences, University of Copenhagen, Denmark

General Observations on the Culture of Lupine (Lupinus mutabilis Sweet) The Andean lupine, locally known as ‘tarwi’ or ‘chocho’ (Lupinus mutabilis Sweet) has been cultivated, processed and consumed for at least 1500 years, whose genetic variability has adapted to many microclimates [1]. Even before the Spanish conquest did this crop play an important role in high Andean production systems and in feeding the indigenous population [2]. Among legumes, the lupine is characterised by its high-quality protein content, suitability *Corresponding author: Marten Sørensen, Department of Plant & Environmental the Andean region, the annual per capita consumption varies, e.g., in Ecuador, it is 4 to 8kg Sciences, University of Copenhagen, for environmentally-1 robust production, and potential-1 health benefits [3]. In the -1countries of Denmark person , much higher than in Bolivia (0.2kg person ) and Peru (0.5kg person ). However,

Submission: April 24, 2021 of approx. 6,000 tons [4]. The gastronomic versatility and nutritional qualities of this legume for the year 2017, production did not meet domestic demand in Ecuador, reporting a deficit Published: June 17, 2021 crop, combined with the work carried out for more than 20 years by both public and private entities in technological innovations, post-harvest, added value, quality seed, improved Volume 1 - Issue 4 varieties, among other aspects, have renewed interest in this cultivation [5-7].

How to cite this article: Doris Introduction (Description, Domestication/Cultivation History, Including Current Cultivation, Geographical Distribution, Uses) Bastidas, Marten Sørensen. The Andean Lupine-‘ElChalampuente-Flores, Chocho’ or ‘Tarwi’ César (Lupinus Tapia Introduction mutabilis Sweet). Biodiversity Online J. 1(4). BOJ.000520.2021. The history of this species as an Andean subsistence crop demonstrates its potential as a crop for low-input agriculture in temperate climates [8]. The selection activities of Andean Copyright@ Marten Sørensen. This farmers have represented the only means of domestication of the lupine, giving rise to semi- article is distributed under the terms of domesticated forms characterized by indehiscent legumes/pods, large seeds, multicolored the Creative Commons Attribution 4.0 International License, which permits unrestricted use and redistribution that can be grown in poor soils and dry climates [1], which stands out for its great potential in provided that the original author and flowers, highly branched architecture and a more or less annual life cycle [9]. It is a robust crop source are credited. content (4.5g 100g-1 dw) [11], the crop has a high resistance to microbial infections and insect soil recovery due to its ability to fix nitrogen [10]. Furthermore, in addition to its high alkaloid attacks [12]. The presence of these alkaloids in the seeds and the low yields (800-1,300kg ha-1) have strongly limited the expansion of this crop [13,14]. Efforts have been made to reestablish lupine as a crop in South America and to adapt it to conditions in Europe [15].

The Andean lupine is characterized by the highest grain quality of all cultivated lupines, presenting an oil content similar to that of soybeans (Glycine max (L.) Merr.) [16]. Numerous

a wide range of possible products ranging from proteins, oils and food additives to cosmetics, studies investigating the nutritional profile and potential applications of this pulse have found medicines and biopesticides. Also, the nutritional advantages make it an ideal product for the transition from meat-intensive diets to diets based on vegetable proteins [16].

Biodiversity Online Journal 1 BOJ.000520. 1(4).2021 2

Origin, diversification and domestication C.P.Sm., L. ballianaus C.P.Sm., L. chlorolepis C.P.Sm., L. condensiflorus C.P.Sm., C.P.Sm., C.P.Sm., Ulbr., The oldest evidence of cultivated Andean lupine is related to L. cuzcensis L. dorae L. eriocladus L. ., ., Desr., the seeds found in tombs of the Nazca culture and representations gibertianus C.P.Sm L. macbrideianus C.P.Sm L. microphyllus L. , Rusby, C.P.Sm. and in Tiahuanaco ceramics in Peru [17,18]. The oldest archaeological paniculatus Desr. L. sufferuginous L. tarapacencis L. tomentosus DC. [21]. evidence of domesticated L. mutabilis seeds has been found in the Mantaro Valley in central Peru and dates back to approx. 1800BP. Germplasm collections The use of RADseq in the analysis of this archaeological material L. mutabilis Blanco at the University of Cusco (Peru) and soon spread to region (northern Peru), from the wild progenitor L. piurensis C.P.Sm. The germplasm collections were started in 1974 by Dr Oscar confirms that was first domesticated in the Cajamarca Demographic analysis suggests that L. mutabilis separated from its more than 3,000 Andean lupine genotypes. The largest and most parent around 2600BC and suffered a bottleneck in domestication, Bolivia and Ecuador; Currently, South American institutions have relevant germplasm collections of L. mutabilis are found in the with subsequent rapid population expansion as it was cultivated gene banks of Peru, Ecuador and Bolivia. However, there are also Lupinus mutabilis is reported in Eastern South smaller collections in Chile, Argentina, Colombia, Australia, Russia, America, from Colombia to northern Argentina, and with a wide in the Andes [19]. Poland, Germany, Spain, Hungary, the United Kingdom and Portugal altitudinal range from 1500 to 3800m a.s.l. [20]. [20]. Regarding the Ecuadorian collection of Lupinus, the National Institute for Agricultural Research (INIAP) has a collection of relatives that show diversity and variability found in the Andean approx. 530 accessions of which about 70% belong to L. mutabilis In the Andean region 83 species have been identified; the wild lupine are the following species: Lupinus ananeanus Ulbr., L. aridulus Sweet (Table 1).

Table 1: Number of accessions of L. mutabilis conserved in the INIAP germplasm bank.

Province No. of Accessions in the Gene Bank* Percentage No. of Collected Accessions** Percentage Altitudinal Range (m a.s.l.) Carchi 10 6.41 14 15.73

Imbabura 14 5 5.62 2597-31722204-3057 Pichincha 14 8.97 4 Cotopaxi 12 8.97 20 22.474.49 2690-35002538-3507 Tungurahua 7 7.69 11 12.36 Chimborazo 76 48.714.49 30 33.71 2600-33902380-3600 Bolívar 2 1.28 - - 2460-2837 Azuay 10 6.41 2 2.25

11 7.05 3 3.37 2450-2918 TotalLoja 156 100 100 1900-2900

Note: Germplasm collected: *period 1975-1999; ** period colour distribution89 also varies among a wide range of patterns, 2014-2015. such as brow-shaped, crescent, mottled or spotted, which can be Botanical description expressed either solitary or in combination [13,24]. Three geographically separated morpho-types of the Andean The presence of considerable variation in germplasm is shown lupine have been suggested based on the considerable genetic by different phenotypic traits, such as a wide range of growth and morphological variability and wide ecological adaptation in the Andean zone: a) Lupinus mutabilis, lupine (northern Peru and periods, branching patterns, colour and shape of grains and flowers, (ISSR) and Single- Sequenced Repeat (SSR) markers have revealed as well as flowering times. Both the Inter-Simple Sequence Repeat of leaves and stems, some ecotypes behave as a biennial, tolerant a broad genetic diversity among L. mutabilis lines [25,26], which Ecuador), of more prolific branching, very late, greater hairiness Lupinus mutabilis, tarwi (central and southern could be related to the mixed pollination system that the species Peru), scarcely branched, moderately late, somewhat tolerant to has, and which could explain the presence of the test colour [25]. to anthracnose; b) Lupinus mutabilis, tauri (highlands of Peru Environments where lupine is grown and Bolivia), smaller (1-1.40m) with a developed main stem, very anthracnose; and c) early, susceptible to anthracnose [13,22,23]. High diversity seed The requirement for lupine is variable, depending on the soil, characteristics include shape (lenticulate to spherical), primary temperature and wind. It grows well in temperatures from 20 to 25 o oC (night temperature), can range from pearly white to solid black and includes beige/ C; grain development is optimal below 9.5 and secondary seed colour, as well as distribution patterns; colour ecotypes of Puno-Peru, needs 450mm of precipitation per crop yellow, brown, dark brown, and colors in between such as brownish a condition that occurs in the high Andean region [23]; the early green and greyish green. Most of the seeds have a secondary colour cycle, while the late ecotypes require between 600 and 700mm [13]. The lupine prefers sandy loam soils, with a thick, deep texture, distribution in darker shades of the primary colour; the secondary

with a balance of nutrients, good drainage with a pH of 5 to 7 faba L.) in the crop rotation system [35]. Studies have demonstrated [21,27,28]. In the seedling stage it is susceptible to frost (-4 °C), the that the Andean lupine can incorporate between 200 and 500kg higher the temperature, the greater the growth and development, nitrogen ha-1 on the contrary, at less than zero degrees Celsius, development and of urea ha-1 into the soil; i.e., an amount equivalent to 350-750kg evapotranspiration are inhibited [18]. converting atmospheric carbon into structural carbon (similar to [43]. This is due to the photosynthetic efficiency in Uses with different species of bacteria and with its ability to solubilise C4 crops), with its ability to fix atmospheric nitrogen in symbiosis phosphorus from the soil [35,44]. an ingredient in different products such as fresh salads, soups, Chocho can be consumed directly as a snack [29] and as Harvest residues are used as green manure, and the dried uses of lupine are related to the extraction of oil and production stems as fuel due to their large amount of cellulose that provides cakes, cookies, bread, hamburgers, baby food [29-32]. The new animal feed [33,34]. Alkaloids such as lupine and sparteine present an excellent calorific value [45]. Something particular that happens of vegetable milk, yoghurt, obtaining flours and by-products for emerges and covers the soil in the plots at rest is a diversity of wild in the leaves, stem and seed of lupine plants were traditionally in Andean ecosystems is that after earthworks, the first thing that relatives of the Andean lupine, which contributes to the recovery of used, in combination with paico (Dysphania ambrosioides (L.)) soil fertility [35]. Mosyakin & Clemants, syn. Chenopodium ambrosioides L., a wild relative of quinoa) to repel pests on potato crops such as the Andes Nutritional aspects weevil (Premnotrypes spp.) and kona kona (Eurysacca quinoae The Andean lupine, compared to other legumes such as P.) the primary pest of quinoa. In livestock, it is used to control soybeans and beans (Phaseolus vulgaris L.), has enormous internal and external parasites, practices that are disappearing nutritional and nutritional potential. The protein content ranges due to the promotion of industrial agrochemicals [35]. Lupine between 40 and 51%, with a high globulin and albumin content, seeds are used for consumption after debittering [30,36] reducing the alkaloid content to 0.02% for people and from 0.4 to 0.6% for oil content (18 to 22%), in which fatty acids such as linolenic and pigs, ruminants and poultry [18,37]. To eliminate antinutritive but it is low in tryptophan; it has calcium, iron, zinc, and a high linoleic predominate (Table 2) [34]. substances (alkaloids), a hydro-thermal process is carried out, which consists of hydrating the dry grain and soaking it for 12 to Table 2: Average of the nutritional and functional 14 hours, then it is cooked for 30 to 40 minutes. The seed is left in components of lupine. a stream of continuous drinking water for three or four days, or in Component Unit Amount circulating water from the river or streams between seven and ten Protein (%) % 51.20 days [38]. Amino Acids Assets/Benefits (Nutrition, Growing Practices, e.g., Valine (g/100g*)

Crop Rotation, etc.) Methionine (g/100g*) 1.490.16 Current situation of lupine in Ecuador Isoleucine (g/100g*) 1.82 The Andean lupine is currently of agricultural importance only Leucine (g/100g*) 2.75 Lysine (g/100g*)

Lipids % 1.79 in Ecuador, -1Peru and Bolivia [39]. The area sown according to the of 400kg ha , however, with the introduction of improved varieties, Fatty Acids III National Agricultural Census was 5974ha, with an average yield 21.9 the yield oscillates between 1500kg ha-1 [4,40]. Data from [41] Linoleic acid % 28.5 Linolenic acid % 2.5 a yield of 3,678kg ha-1. The lupine is produced in the altitudinal report a sown area of 3,642ha, with a production of 1,339 tons and % 13.5 strip that goes from 2500m a.s.l., parallel to the cereal area, up to Calcium Fibre % 0.37 provinces where production is centred are Cotopaxi, Chimborazo Phosphorous % 0.43 3400 or 3600m a.s.l. with risks of frost and hailstorms [37]; the and Pichincha [40]. Ecuador has two improved varieties of Andean Magnesium % 0.05 lupine: INIAP 450 ‘Andino’ and INIAP 541 ‘Guaranguito’ from Iron µ/g 61.00 Peruvian lines that have a short crop cycle (6 months) and a high Zinc µ/g alkaloid content [42]. Note: *Content per 100g fresh sample. 92.00 Crop husbandry Source: [34]. In the highlands of Colombia, Ecuador, Peru, Bolivia and Chile, Linoleic acid has properties, which in human metabolism are the Andean lupine and its wild relatives (kela or kera) constitute one of the components of agroecosystems and ecosystems. The consumption of Andean lupine decreased notably since colonial unique and irreplaceable during specific stages such as pregnancy and lowers blood pressure, while oleic acid reduces the risk of times because it was replaced by the introduced broad bean (Vicia and the first months of postpartum life. Also, it increases defences

cardiovascular disease and is antitumor [46]. It prevents chronic iii. Converting production into a dual-purpose alternative (protein diseases such as diabetes, gout, kidney problems, diuretic and and oil) similar to soybean could be an economical alternative emollient [47], it also has antioxidant properties due to the for the productive and competitive development of the Andean region [3].

Limitations:presence of isoflavones Reproduction [25]. Needs iv. Andean lupine alkaloids could be of commercial importance From an agronomic point of view due to their pharmacological activity [12,52]. Furthermore, i. One limitation is the lack of early maturing and high-yielding commercial importance due to their functional properties for genotypes, the lack of locally adapted genotypes [15], and the specific protein isolates and concentrates could be of

the chemical and food industry [11,53-55]. Furthermore, the [56] increases the nutritional value of this culture by offering a ii. lackLimited of good research quality in seed plant production breeding: [39]. recent domestication presence of ferritine (protein-rich in Fe) in the protein profile safe way to increase the intake of iron in the diet [57]. and history of reproduction fragmented in time and space have also contributed to the lack of genetic improvement and v. have an essential role due to multiple properties such as the selection of local ecotypes. Besides, the lack of advanced In the medical field, quinolizidine alkaloids (Qas) also lower yields; lack of participatory approaches with farmers for biotechnological methods in genetics, molecular cytogenetics antiarrhythmic, anti-inflammatory, diuretic and hypotensive or tissue culture, has limited the possibility of exploiting natural application in agriculture as a bio-stimulant increasing the variability and performing distant crosses and haploidisation effects among others [58]. Besides, QAs can also find of material from reproduction [16]. [60] or as biocidal agents that replace synthetic toxins [61]. growth and yield of other crops [59], as antibacterial agents iii. Presence of phytophagous insects: in Ecuador, the increase References 1. Andean lupine, with the use of improved varieties and broader & Hall, London, U.K. in demand intensified the ancestral production system of Haq N (1993) Underutilized crops. In pulses and vegetables. Chapman cultivated areas, which caused the presence of these insects 2. and the indiscriminate use of insecticides [48]. latin america and the caribbean compared to more commercial crops. FAO (2016) Legume consumption and production has lost strength in From a nutritional point of view 3. i. The Andean lupine has a bitter taste as a result of the high SciLucas 6: 1-6.MM, Stoddard F, Annicchiarico P, Frias J, Martinez-Villaluenga C, et al. (2015) The future of lupin as a protein crop in Europe. Front Plant content of alkaloids, which limits direct consumption for both 4. Mazón N (2018) Chocho or tarwi as a genetic resource in the Andean

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